conflicts of interest in gm bt crop efficacy and

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Conflicts of interest in GM Bt crop efficacy anddurability studies

Thomas Guillemaud, Eric Lombaert, Denis Bourguet

To cite this version:Thomas Guillemaud, Eric Lombaert, Denis Bourguet. Conflicts of interest in GM Bt crop effi-cacy and durability studies. PLoS ONE, Public Library of Science, 2016, 11 (12), �10.1371/jour-nal.pone.0167777�. �hal-01602436�

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RESEARCH ARTICLE

Conflicts of Interest in GM Bt Crop Efficacy and

Durability Studies

Thomas Guillemaud1☯*, Eric Lombaert1, Denis Bourguet2☯

1 Inra, Univ. Nice Sophia Antipolis, CNRS, UMR 1355–7254 Institut Sophia Agrobiotech, Sophia Antipolis,

France, 2 Inra, UMR 1062 Centre de Biologie pour la Gestion des Populations (CBGP) Inra-IRD-CIRAD-

Montpellier SupAgro, 755 avenue du Campus Agropolis, CS, Montferrier / Lez cedex. France

☯ These authors contributed equally to this work.

* [email protected]

Abstract

Public confidence in genetically modified (GM) crop studies is tenuous at best in many coun-

tries, including those of the European Union in particular. A lack of information about the

effects of ties between academic research and industry might stretch this confidence to the

breaking point. We therefore performed an analysis on a large set of research articles (n =

672) focusing on the efficacy or durability of GM Bt crops and ties between the researchers

carrying out these studies and the GM crop industry. We found that ties between research-

ers and the GM crop industry were common, with 40% of the articles considered displaying

conflicts of interest (COI). In particular, we found that, compared to the absence of COI, the

presence of a COI was associated with a 50% higher frequency of outcomes favorable to

the interests of the GM crop company. Using our large dataset, we were able to propose

possible direct and indirect mechanisms behind this statistical association. They might nota-

bly include changes of authorship or funding statements after the results of a study have

been obtained and a choice in the topics studied driven by industrial priorities.

Introduction

Despite the extraordinary financial, political and ideological stakes relating to genetically mod-

ified (GM) crops, we were able to identify only two research studies [1, 2] focusing on conflicts

of interest (COIs)—defined as “a set of circumstances that creates a risk that professional judg-ment or actions regarding a primary interest will be unduly influenced by a secondary interest”[3]—in this field of research. These two studies reported similar frequencies of COIs in

research articles on GM crops, but differed markedly in their conclusions. Sanchez [1] con-

cluded that COIs were not frequent enough to be a serious issue in GM crop studies, whereas

Diels et al. [2] warned that COIs might be a problem because they were significantly linked to

study outcomes. Unfortunately, one of these studies was potentially subject to COI itself [1]

(the author’s affiliation was ChileBio, http://www.chilebio.cl, which is funded by companies

that develop GM crops) and the other included a limited number of articles [2] (n = 94).

We investigated the occurrence of COIs in GM crop studies and their association with the

outcome of those studies further, by analyzing 672 full-text articles focusing on two topics: the

PLOS ONE | DOI:10.1371/journal.pone.0167777 December 15, 2016 1 / 14

a11111

OPENACCESS

Citation: Guillemaud T, Lombaert E, Bourguet D

(2016) Conflicts of Interest in GM Bt Crop Efficacy

and Durability Studies. PLoS ONE 11(12):

e0167777. doi:10.1371/journal.pone.0167777

Editor: Raul Narciso Carvalho Guedes,

Universidade Federal de Vicosa, BRAZIL

Received: July 22, 2016

Accepted: November 2, 2016

Published: December 15, 2016

Copyright: © 2016 Guillemaud et al. This is an open

access article distributed under the terms of the

Creative Commons Attribution License, which

permits unrestricted use, distribution, and

reproduction in any medium, provided the original

author and source are credited.

Data Availability Statement: All relevant data are

within the paper and its Supporting Information

files.

Funding: The authors received no specific funding

for this work.

Competing Interests: The authors have declared

that no competing interests exist.

http://www.chilebio.cl/

http://crossmark.crossref.org/dialog/?doi=10.1371/journal.pone.0167777&domain=pdf


efficacy and durability of GM crops producing Bacillus thuringiensis (Bt) toxins–often referred

to as Bt crops–against target pest insects (see the flowchart of article selection in Fig 1 and S1

Table for a list of all the articles, with the associated classifications).

The efficacy and durability of Bt crops are defined here as the level of pest control provided

by the Bt toxin they produced or by the crop themselves and the sustainability of this pest con-

trol over time, respectively.

Fig 1. Flowchart diagram describing how literature was gradually included/excluded in the analysis. The details of the protocol of literature

inclusion and exclusion are described in the material and methods section.

doi:10.1371/journal.pone.0167777.g001

Conflicts of Interest in GM Bt Crop Studies


We used the COIs created by ties with GM crop companies as a model of COIs for this

study because the best interests of these companies was easy to characterize (efficacy and dura-bility of the crops) and COIs were easy to detect (affiliation of an author to a GM crop com-

pany or part of the funding provided by a GM crop company).

Materials and Methods

Goal of this study

We explored the occurrence of COIs and the association between COIs and outcomes in stud-

ies of genetically modified (GM) crops. We focused our analysis on articles evaluating the effi-cacy or durability of GM crops producing toxins (Cry and Vip proteins) from Bacillusthuringiensis (Bt) against targeted pests. These articles included studies on the main Bt crops

developed by Monsanto (e.g. maize and cotton varieties expressing the MON810 and

MON1076 events, respectively), Syngenta (e.g. maize varieties expressing the Bt11 event), Dow

AgroSciences and DuPont Pioneer (e.g. maize varieties expressing the 59122 event).

We used the COI created by the professional affiliation of authors to GM crop companies

or the provision of funding for the study by these companies as the model of COI for this

study. We considered only COIs linked to GM crop companies because the best interests of

these companies were easy to characterize (efficacy and durability of crops) and the presence of

such COIs was easy to detect (an author was affiliated to a GM crop company or some of the

funding came from a GM crop company). The COIs investigated here correspond therefore to

financial COIs. Non-financial COIs [4], also known as intrinsic COIs or intellectual COIs,

were not investigated.

The goal of this study was 1) to measure the extent of COIs in this field of research, 2) to

test the hypothesis that study outcomes for the efficacy or durability of Bt crops are more fre-

quently favorable to the interests of GM crop companies in the presence than in the absence of

COIs and 3) to investigate the mechanisms underlying the association between COIs and

study outcomes.

Article selection–first step

The flowchart describing the literature included/excluded is shown in Fig 1. We initially

selected articles by searching the Web of Science (WoS, ISI Web of Knowledge, Thomson Sci-

entific) bibliographic database. We used a Boolean search term including (1) most crops (e.g.

cotton, maize, potato) for which GM varieties producing Bt toxins have been commercialized,

and (2) most of the pests targeted by Bt crops (e.g. Diabrotica virgifera virgifera, Ostrinia nubi-lalis, Pectinophora gossypiella).

The exact Boolean search term was:

((TI = (rootworm� OR Diabrotica OR borer� OR Ostrinia OR Diatraea OR armyworm�

OR Spodoptera OR stalkborer� OR Busseola OR Sesamia OR bollworm� OR Helicoverpa OR

earworm� OR Leafworm� OR Pectinophora OR budworm� OR Heliothis OR "Colorado

potato beetle" OR "Colorado potato beetles" OR Leptinotarsa OR Chrysomela OR "Cotton-

wood beetle" OR "Cottonwood beetles" OR "Diamondback moth" OR "Diamondback moths"

OR Plutella OR "Rice leaf folder" OR "Rice leaf folders" OR Cnaphalocrocis OR "Chilo suppres-

salis" OR "Leucinodes orbonalis" OR "Soybean looper" OR "Soybean loopers" OR "Pseudoplu-

sia includens") AND TS = (maize� OR corn� OR "Zea mays" OR cotton� OR "Gossypium

hirsutum" OR soybean� OR "Glycine max" OR potato� OR "Solanum tuberosum" OR poplar�

OR Populus OR eggplant� OR "Solanum melongena" OR brinjal� OR tomato� OR "Lycopersi-

con esculentum" OR rice OR "Oryza sativa" OR broccoli� OR "Brassica oleracea" OR tobacco�

OR nicotiana) AND TS = ("bt" OR cry� OR bacillus OR toxin�) AND TS = (transgenic� OR



GMO� OR GMP� OR "genetically modified" OR "Bt crop" OR "Bt plant" OR "Bt tree")) OR (TS

= ("western corn rootworm" OR "Diabrotica virgifera" OR "European corn borer" OR "Asian

corn borer" OR "Southwestern corn borer" OR "Ostrinia nubilalis" OR "Ostrinia furnacalis"

OR "Diatraea grandiosella" OR "Diatraea saccharalis" OR "Sugarcane Borer" OR "fall army-

worm" OR "Spodoptera frugiperda" OR "African maize stalkborer" OR "Busseola fusca" OR

"Sesamia nonagrioides" OR "Mediterranean corn borer" OR "Australian bollworm" OR "Heli-

coverpa punctigera" OR "Helicoverpa zea" OR "Spodoptera littoralis" OR "Corn earworm" OR

"Cotton Leafworm" OR "Pink bollworm" OR "Cotton bollworm" OR "Pectinophora gossy-

piella" OR "Helicoverpa armigera" OR "Tobacco budworm" OR "Heliothis virescens" OR "Col-

orado potato beetle" OR "Leptinotarsa decemlineata" OR "Chrysomela tremulae" OR

"Chrysomela scripta" OR "Cottonwood beetle" OR "Diamondback moth" OR "Plutella xylos-

tella" OR "Rice leaf folder" OR "Cnaphalocrocis medinalis" OR "Striped stem borer" OR "Chilo

suppressalis" OR "Leucinodes orbonalis" OR "Fruit Borer" OR "Shoot Borer" OR "Soybean

looper" OR "Pseudoplusia includens") AND TI = (maize� OR corn� OR cotton� OR soybean�

OR potato� OR poplar� OR eggplant� OR brinjal� OR tomato� OR rice OR broccoli� OR

tobacco�) AND TI = ("bt" OR cry� OR bacillus OR toxin�) AND TS = (transgenic� OR GMO�

OR GMP� OR "genetically modified" OR "Bt crop" OR "Bt plant" OR "Bt tree")))

We searched the WoS database on September 11, 2015. Using the above search term and

limiting the query to articles published in English between 1990 and 2015, we recovered 1,227

articles.

Two of us (DB and TG) then independently screened the titles and abstracts of these 1,227

articles, to eliminate those beyond the scope of our survey. Articles that were classified either

with uncertainty by at least one of us (4.6%) or differently (7.9%) were jointly discussed to

reach a consensus. We excluded 307 articles which dealt with various subjects, including

assessments of the effects of Bt crops on non-target organisms, GM crops producing toxins

other than those from Bt (e.g., toxins from spiders, lectins) and Bt crops developed by academ-

ics rather than by GM crop companies.

Classification by the type of conclusion

The outcomes of the 920 articles retained for the analysis were classified as ‘favorable’, ‘neutral’or ‘unfavorable’ to the financial interests of at least one GM crop company. This classification

was done independently by two of us (DB and TG) and was based exclusively on the titles and

abstracts of the articles, with no knowledge of the authors’ names and affiliations or of funding

sources. This classification was also preformed independently of the classification on the basis

of study topic. Articles that were classified either with uncertainty by at least one of us (11.2%)

or differently (19.6%) were jointly discussed to reach a consensus.

Articles were classified on the basis of the general tone of the title and abstract and the for-

mal conclusions given in the abstract, on the basis of the following criteria:

1. Favorable if the article reported that:

a. One or several of the Bt crops tested provided a satisfactory level of control of the tar-

geted pests;

b. The susceptibility of the targeted pest populations to Bt toxins was high and/or remained

unchanged over time (i.e. indicating an absence of evidence for the selection of mecha-

nisms of resistance to the Bt toxins produced by Bt crops);

c. Laboratory selection did not yield individuals sufficiently resistant to develop on Btcrops;



d. Biotic and abiotic factors (relating to the pests and/or the plants) provided favorable con-

ditions for the management of Bt resistance in targeted pests (e.g. Bt crops produced

high doses of toxins, Bt resistance was recessive and/or associated with fitness costs,

non-Bt crops (called refuges) were planted in sufficient quantities and sufficiently close

to Bt crops);

e. Pest populations resistant to a particular Bt toxin were controlled by another toxin or by

other methods for which there was no cross resistance;

f. Several Bt toxins acting via different receptors (i.e. decreasing the risk of cross-resistance)

could be successfully combined in Bt crops through pyramiding.

2. Neutral if the article reported:

a. Theoretical models exploring the influence of virtual biotic and abiotic conditions on the

selection of Bt resistance in targeted pest populations;

b. The development of monitoring tools for following the susceptibility of targeted pest

populations to Bt crops;

c. The baseline susceptibility of pest populations before the cultivation of Bt crops targeting

those populations;

d. Receptors for Bt toxins and/or mechanisms or genetic changes conferring resistance to

these toxins in the targeted pest populations.

3. Unfavorable if the articles reported that:

a. One or several Bt crops did not provide a high level of control of the targeted pests,

potentially jeopardizing the efficacy of the Bt resistance management strategy;

b. The susceptibility to Bt toxins decreased and/or Bt resistance developed in the targeted

populations (in either laboratory or natural conditions);

c. Resistance to one Bt toxin in the targeted pest populations jeopardized the successful use

of other toxins to control those populations (i.e. the occurrence of cross-resistance);

d. Biotic and abiotic factors (relating to the pest and/or the plant) created unfavorable con-

ditions for the management of Bt resistance in the targeted pests (e.g. Bt crops did not

provide high doses of toxins, Bt resistance was not fully recessive and/or was not associ-

ated with fitness costs, non-Bt crops (i.e. refuges) were planted in insufficient quantities

and/or too far away from Bt crops).

Article selection–second step

We were able to retrieve PDF files containing the whole content of the article for 893 of the 920

articles classified by the type of conclusion. These 893 PDF files were screened independently

by two of us (DB and TG) to check again the relevance of the papers for this study. Articles that

were classified either with uncertainty by at least one of us (5.4%) or differently (5.7%) were

jointly discussed to reach a consensus. We identified 672 of these articles as relevant (S1 Table).

Classification by topic

The 672 articles retained were classified into two categories on the basis of the topic consid-

ered: the ‘Efficacy’ or ‘Durability’ of the GM crops studied. This classification was done



independently by two of us (DB and TG) and was based on titles and abstracts only, blind to

the names and affiliations of the authors and to sources of funding (see below). Articles that

were classified either with uncertainty by at least one of us (25.1%) or differently (4.3%) were

jointly discussed to reach a consensus.

Papers assigned to the Efficacy category reported data on:

1. Plant toxicity;

2. Control of the targeted pests;

3. Yield performance;

4. The baseline susceptibility of targeted species;

5. The efficacy of new toxins;

6. New methods of toxin combination;

7. The economic advantages of GM plant use.

Papers assigned to the Durability category reported data on:

1. The selection of target pest strains resistant to Bt toxins in the laboratory;

2. The initial frequencies of Bt resistance alleles within natural populations of the targeted

pests;

3. The detection of Bt resistance within natural populations of the targeted pests;

4. Changes in the efficacy of Bt crops over time;

5. Resistance characteristics (number of genes involved, inheritance, dominance, epistasis,

pleiotropy) of the targeted pests;

6. The development of strategies for limiting/preventing the evolution of Bt resistance (e.g.

the high-dose/refuge strategy) of the targeted pests;

7. Tests of the assumptions underlying such strategies.

Classification by funding source and author affiliation

We also analyzed the authors’ professional affiliations and the funding sources (see below) of

the 672 articles retained for the analysis. This analysis was again performed independently by

two of us (DB and TG) blind to the classification of the article for topic and study outcome, as

described above. Articles that were classified either with uncertainty by at least one of us (2.1%

and 13.7% for authors’ affiliations and the funding sources, respectively) or differently (5.5%

and 10.1% for authors’ affiliations and the funding sources, respectively) were jointly discussed

to reach a consensus.

For each paper, we recorded:

1. The presence or absence of authors professionally affiliated to a GM crop company. This

was established by screening the address of each author appearing in the authors’ affiliation

section of the article;

2. For publications co-authored by academics and one or more authors professionally affili-

ated to a GM crop company, whether the senior author worked for a GM crop company or

was an academic researcher. The senior author was identified as the corresponding author

for the paper;



3. Whether the sources of funding were declared. In cases in which the funding sources were

declared, we distinguished between funding from GM crop companies (partial or complete)

and funding from other sources (governmental agencies, non-profit organizations, founda-

tions, universities, etc.).

Using this information, we determined, for each article, whether there was:

1. An affiliation COI, defined as the presence of at least one author from a GM crop company

on the paper;

2. A funding COI, defined as at least partial funding for the study from a GM crop company.

Overall, a paper was considered to display COI if it displayed either an affiliation or a fund-ing COI.

Leading authors

For each article, the leading author was identified as the author present on the largest number

of papers from among the 672 papers considered in this analysis. If several authors of a given

paper had been authors on the same number of articles in our list, the leading author was iden-

tified as the first in alphabetic order. We identified 193 leading authors in total (mean number

of papers per leading author = 3.48, median = 14.4, minimum = 1, maximum = 53, 5th percen-

tile = 1, 95th percentile = 15)

Statistical analysis

The associations between (i) the presence/absence of COI and study outcome, (ii) the pres-

ence/absence of COI and the topic of the article, and (iii) the topic of the article and its out-

come, were assessed in Fisher’s exact tests, with the function fisher.test of R [5].

For a given article, the effect of its topic (i.e. efficacy or durability) on its number of citations

(TC), as recorded on September 11, 2015 in the WoS, was evaluated with a mixed linear

model, using the lmer function of R. The data were normalized by log(TC+1) transformation.

The number of authors was included as a fixed effect and the identity of the leading author of

each article was treated as a random effect. The age of the paper (i.e. 2015 minus the year of

publication) was also considered as a fixed effect.

For a given author and a given topic, we evaluated the effect of COI on study outcome, by a

generalized linear mixed model approach, with the glmer function of R (library lme4). The

topic of the article and COI were considered as fixed effects and the identity of the leading

author was treated as a random effect. The outcome of the study was considered as a binary

variable with levels ‘favorable’ and ‘other’ (containing both ‘neutral’ and ‘unfavorable’ catego-

ries). We used the Akaike information criterion (AIC) [6] to select the best model.

Direct and indirect COI links

The global link between COI and the probability of obtaining a positive outcome can be writ-

ten as follows:

D ¼ PðþjCOIÞ � Pðþjno COIÞ

¼ Pðt 1jCOIÞPðþjt 1;COIÞ þ Pðt 2jCOIÞPðþjt 2;COIÞ

� Pðt 1jno COIÞPðþjt 1; no COIÞ þ Pðt 2jno COIÞPðþjt 2; no COIÞ

where t1 and t2 are the two topics and + within the brackets indicates a positive outcome. In



the absence of direct COI links, i.e. when

Pðþjt1;COIÞ � Pðþjt1; no COIÞ ¼ Pðþjt2;COIÞ � Pðþjt2; no COIÞ ¼ 0;

then

Dindirect link ¼ ðPðt1jCOIÞ � Pðt1jno COIÞÞðPðþjt1;COIÞ � Pðþjt2;COIÞÞ

In the absence of indirect COI links, i.e. when

Pðt1jCOIÞ � Pðt1jno COIÞ ¼ 0;

then

Ddirect link ¼ Pðt1jCOIÞðPðþjt1;COIÞ � Pðþjt1; no COIÞÞ

þð1 � Pðt1jCOIÞÞðPðþjt2;COIÞ � Pðþjt2; no COIÞÞ

Results and Discussion

A widespread occurrence of COI

Like Sanchez [1] and Diels et al. [2] we found that COIs were widespread in the articles consid-

ered (Fig 2). Only about 7% (n = 46) of the articles contained a declaration of COI, but about

one fifth (n = 141) of the 672 articles had at least one author from a GM crop company. Details

about funding were provided by 524 articles, 29% (n = 153) of which acknowledged financial

support from a GM crop company. By combining information about authors’ affiliations and

funding statements, we were able to assess the presence or absence of COI for a total of 579

articles (Table 1), 40% of which (n = 229) presented COIs. This figure is intermediate between

those reported by Sanchez [1] (25.8%) and Diels et al. [2] (47%).

A significant association between COI and study outcome

For the 579 articles we were able to classify, we found that COIs were associated with a 49%

higher frequency of outcomes favorable to the interests of the GM crop company (p = 4x10-5,

Fig 3A). Such an association between COI and study outcome was also reported by Diels et al.[2] and has been identified in other fields, including those of tobacco [7], biomedical [8],

nuclear [9], sugar [10] and pharmaceutical [11] research. However, the mechanisms underly-

ing this association have been little investigated. We studied these mechanisms in more detail.

The best model describing the outcomes of the studies was that with all fixed (Topic and COI)

and random (leading author) effects but no term for interaction between Topic and COI effects.

The main factor was Topic, with efficacy leading to a favorable outcome in 61% of cases, whereas

only 30% of articles on durability resulted in a favorable outcome (p = 8x10-16). The second most

important factor was the presence of a COI, which increased the probability of a favorable out-

come by +26% for articles on efficacy and +50% for articles on durability, respectively

(p = 2.2x10-3). The leading author’s identity had an effect of only marginal significance (p = 0.07).

This model suggests the existence of direct and indirect links between outcome and COI.

Direct and indirect links between outcome and COI

First, we detected an indirect link between outcome and COI through the topics studied. Studies

with COIs investigated efficacy 70% more frequently than studies without COI (p = 3.8x10-7, Fig

3B). Moreover, outcomes were 104% more likely to be favorable for articles focusing on efficacythan for those exploring durability (Fig 3C, p = 8x10-16). This would naturally lead to, and,

therefore, partly explain, the association between COI and favorable outcome.



Second, we found a direct link between outcome and COI within each topic. For a given lead-

ing author and a given topic, study outcomes were more likely to be favorable to the GM crop

company in the presence than in the absence of COI (+26%, p = 0.05 for efficacy, +50%, p = 0.02

Fig 2. Occurrence of COI in GM crop studies. (A) Distribution of declarations of COI over time between 1991 and 2015, in 672 articles focusing on the

efficacy or durability of GM crops producing Bacillus thuringiensis toxins against target pest insects; (B) Distribution of COI over time between 1991 and 2015;

(C) Frequencies of the various affiliations; (D) Frequencies of funding categories.


Table 1. Number of articles dealing with the efficacy and the durability of GM Bt crops classified according to their topic—durability and efficacy

—, their outcome—favorable, neutral or unfavorable to the financial interests of GM crop companies—, and their conflicts of interests (COI)—

absence, presence or not determined.

Durability Efficacy

Favorable Neutral Unfavorable Favorable Neutral Unfavorable

Absence of COI 69 93 83 57 31 17

Presence of COI 42 40 30 81 27 9

COI not determined 6 12 17 33 16 9

doi:10.1371/journal.pone.0167777.t001



for durability, and p = 2.3x10-3 overall, Fig 3D). The statistical effect of COI on outcome (i.e. the

difference of probability of obtaining a positive outcome with and without conflict of interest) via

this direct link (Δdirect link = 0.12) was twice that via the indirect link (Δindirect link = 0.07). Numeri-

cal computation of the whole effect, gives Δ = 0.18. Note that Δindirect link + Δdirect link > Δ simply

because of an interaction term.

A cause or a consequence of COI?

Part of the observed COIs may be due to the favorable outcomes. For instance, authorship or

funding statements may be modified after the results of a study have been obtained. GM crop

companies may prefer not to be listed as having provided support for studies leading to unfa-

vorable outcomes. Alternatively, academics might be more inclined to propose researchers

Fig 3. Articles’ outcomes, topics and conflicts of interests. (A) Distribution of article outcomes—favorable, neutral or unfavorable to the financial interests

of GM crop companies—in the presence (n = 229) or absence (n = 350) of COI. Note that 93 articles could not be classified for the presence/absence of COI.

(B) Distribution of the two topics—durability and efficacy—considered by articles in the presence and absence of COI. (C) Distribution of the outcomes of the

672 articles considered, by topic. (D) Probability, for a given author, of a paper reporting an outcome favorable to the financial interests of the GM crop

company, by topic and the presence or absence of COI. The P-values presented are those for Fisher’s exact tests in (a), (b), and (c) and for ANOVA between

GLMs in (D). The number of articles is shown above the bars.




from GM crop companies as co-authors on publications presenting results favorable to the

interests of the company.

Conversely, COIs may be partly responsible for the favorable outcomes, for at least two rea-

sons: (i) GM crop companies may promote research on efficacy rather than durability, thereby

indirectly increasing the frequency of favorable outcomes for papers with COI. The interests

of the scientific community at large seem to be different, as studies without COI focused

mostly on durability, and on average, peer scientists cited durability papers more frequently

than efficacy papers (between +23% and +51%, p = 9.7x10-3, depending on the number of

authors, the leading author and the year of publication, Fig 4). (ii) Data against the interests of

GM crop companies may be less likely to be published in the presence than in the absence of

COI. This scientific bias might underlie the direct link between favorable outcome and COI

found in our study. However, as previously reported by Krimsky [12], this direct link is not

necessarily the consequence of such a bias. Here, studies displaying COI might have investi-

gated more effective and durable GM crops than those without COI, or they may have used

different methodologies (e.g. laboratory vs. field conditions). A closer examination of studies

on GM crops is required to determine which of these possibilities actually accounts for the

direct link between COI and outcome.

Limitations of this study

This study has several limitations. First, we explored only two characteristics of Bt crops: effi-cacy and durability. Other characteristics and consequences of these transgenic plants, includ-

ing all those relating to the environment (e.g. the impact of Bt crops on non-target insects) or

health, merit a similar analysis. As a demonstration of the absence of such effects, rather than

their presence, is clearly in the GM crop companies’ interests, an association between COIs

Fig 4. Number of citations (TC) per article (in September 2015), by topic and year of publication. The p-value

of a common slope for the topics (durability and efficacy) derives from a mixed linear model in which log(TC+1) is

fitted to the age of the paper (i.e. 2015 minus the year of publication, p = 2x10-16), the topic (p = 0.010), and the

number of authors (p = 4.5x10-6) as fixed effects and the identity of the leading author of each article as a random

effect (p = 4.3x10-9).




and the outcomes of studies studying environmental or health impacts is also a testable

hypothesis. Sanchez [1] and Diels et al. [2] focused on studies on health impacts, in which they

found COIs to be very frequent, and Diels et al. [2] found an association between financial or

professional COIs and research outcomes.

Second, as we used the addresses of authors to identify their affiliations, only one type of

affiliation, that relating to employment, was considered. However, authors may have affilia-

tions to GM crop companies of other types, such as being members of advisory boards, consul-

tants, or co-holders of patents [13], and this could also have a significant impact on the

outcomes of studies on GM crops. We did not consider these affiliations as they are not usually

reported in articles (COI statements became obligatory in some journals only recently and, as

revealed here, they remain very rare). The consideration of other types of affiliation would

require a survey that would be difficult to perform given that more than 1,500 authors were

considered in this study.

Third, we have considered only the links between authors and GM crop companies. Other

stakeholders (e.g. Greenpeace, The Non-GMO Project, The Organic Consumers Association,

The Network of European GMO-free Regions) oppose GM crop companies in being openly

against the use of GM crops. An inverse relationship might therefore be expected between the

outcomes of studies on GM crops and the presence of COIs relating to these stakeholders. We

were unable to test this hypothesis because we identified no financial interests connected with

anti-GMO stakeholders, in terms of the professional affiliation of the authors or their declared

funding sources.

Finally, this study focused exclusively on financial COIs. Non-financial COIs, also known

as intrinsic or intellectual COIs — due to personal, political, academic, ideological, or religious

interests — might also have a significant impact on the outcomes of research studies [4]. It is

difficult to decipher intellectual COIs and, as for the detection of non-professional affiliations

with GM crop companies, it would be a major challenge to perform such an analysis given the

large number of authors considered.

We think (although this hypothesis has yet to be tested in this field) that adding studies to

overcome these limitations would have resulted in the same qualitative conclusions: COIs are

frequent, and there is a link between COIs and study outcomes. It remains unclear whether

this would increase the power of the analysis, mostly because some of the abovementioned fac-

tors (stakeholders other than GM crop companies, non-professional affiliations to GM crop

companies and non-financial COIs) might be difficult to classify and would be subject to con-

siderable background noise.

Policy implications

Scientific journals should make it obligatory for authors to publish a COI statement, as such

statements remain too rare (Fig 2A). However, COI statements are not a panacea and do not

absolve scientists and industrial partners of their obligation to deal with COIs [14]. It is almost

impossible to avoid non-financial COIs, but it does seem to be possible to limit the occurrence

of professional and funding COIs in studies investigating the performance and impact of GM

crops. However, it is desirable for these studies to be at least partly funded by GM crop compa-

nies, because these companies are the principal beneficiaries of these products and should take

responsibility for the impact of their products on the environment and health. One way of

combining the possibility of GM crop company funding with an absence of professional and

funding COIs would be a system of indirect financial support for research from the industry:

GM crop companies and other stakeholders (governments, NGOs) would make a financial

contribution to a common pot managed by an independent agency. This agency would launch



and fund calls for proposals developed by researchers and stakeholders, to which researchers

could respond. Projects would be accepted or rejected by a scientific committee independent

of the stakeholders and as free from COIs as possible. With this system, which has already

been proposed for biomedical research [15–17], there would be no direct interaction between

GM crop companies and researchers: COIs due to professional affiliations and funding sources

would be avoided and the continuity of research funding would be independent of the publica-

tion of results favorable or unfavorable to the interests of the companies.

Supporting Information

S1 Table. List of the 672 articles with outcomes classified as favorable, neutral or unfavor-able, topics categorized as efficacy or durability and with affiliation and funding COI char-

acteristics.

(XLSX)

Acknowledgments

Data are available in S1 Table. We would like to thank C. Brouat, V. Calcagno, T. Candresse,

B. Facon, X. Fauvergue, and T.W. Sappington for their comments and insights on drafts of this

manuscript and two reviewers for their valuable comments on a previous version of this manu-

script. We would like to thank Sheldon Krimsky and David Resnik for valuable comments on

an earlier version of the article.

Author Contributions

Conceptualization: TG DB.

Formal analysis: TG EL DB.

Investigation: TG EL DB.

Methodology: TG DB.

Supervision: TG DB.

Writing – original draft: TG EL DB.

Writing – review & editing: TG EL DB.

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